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Modelling buoyancy regulation in fishes

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Article in Ecological Modelling July 2005
DOI: 10.1016/j.ecolmodel.2004.12.013

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Ecological Modelling 185 (2005) 309327

Modelling buoyancy regulation in fishes with swimbladders:

bioenergetics and behaviour
Espen Strand a, , Christian Jrgensen a , Geir Huse b
a

University of Bergen, Department of Biology, P.O. Box 7800, N-5020 Bergen, Norway
b Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway

Received 18 June 2004; received in revised form 13 December 2004; accepted 17 December 2004

Abstract
We present a bioenergetic model for buoyancy regulation that incorporates the restrictions and costs of swimbladder regulation
with four means of hydrodynamic lift production: hovering, swimming with extended pectoral fins, swimming with adjusted tilt
angle, and body lift. Previous models addressing vertical migration in fish with swimbladders have either assumed no energetic
cost or a static cost of vertical migration. In this model, parameterised for Atlantic cod Gadus morhua, existing theory and
experimental data on bioenergetics, physiology, and hydromechanics are integrated. Trade-offs and limitations were investigated
from a behavioural perspective. Regulation of swimbladder volume is energetically cheap but slow. Because of the asymmetry in
absorption and secretion rates with depth, fish that perform vertical migrations regularly will often be negatively buoyant and will
therefore experience additional energy costs associated with hydrodynamic lift production. Hovering was optimal for slightly
negatively buoyant fish, whereas tilted compensatory swimming was optimal in all other situations. The predicted optimal tilt
angle was approximately 7 , and increased for small fish and for fish that were close to neutrally buoyant. The energetic saving
from tilting was small for cod, and potential conflicts with other behaviours may determine when tilting would be preferential in
nature. Swimbladder volumes and the corresponding energetic costs were calculated for constructed vertical migration patterns
and on a set of depth data from a free-living cod. For the free-living cod, the model predicted that the fish would be neutrally or
negatively buoyant, with the swimbladder being up to 40% smaller than the optimal volume.
2005 Elsevier B.V. All rights reserved.
Keywords: Atlantic cod (Gadus morhua); Bioenergetics model; Buoyancy regulation; Physoclist swimbladder; Tilt angle; Vertical migration;
Target strength

1. Introduction

Corresponding author. Tel.: +47 55 58 44 38;

fax: +47 55 58 44 50.
E-mail address: Espen.Strand@bio.uib.no (E. Strand).

0304-3800/$ see front matter 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.ecolmodel.2004.12.013

Living tissue is, with the exception of lipids, heavier than water. Aquatic organisms that intend to utilise
the free water masses will therefore have to adopt
some mechanism by which to control buoyancy. Nature

310

E. Strand et al. / Ecological Modelling 185 (2005) 309327

displays a variety of solutions to this problem, ranging

from constant activity via large deposits of lipids and
oils, to elaborate gas-filled structures (Jobling, 1995;
Schmidt-Nielsen, 1997). The degree to which some
of these adaptations require energy or restrict the behavioural repertoire outlines the magnitude of the selection pressures that have shaped them (Harden Jones,
1951, 1952; Alexander, 1971, 1990, 2003; SchmidtNielsen, 1997).
The swimbladder found widely among teleost fishes
is one solution to the buoyancy challenge. Bloodborne gases are secreted into a gas-filled cavity through
a reaction that requires energy, but maintenance is
energetically cheap once the gases are inside (e.g.
Scholander, 1956; Prosser, 1973; Harden Jones and
Scholes, 1985). The physical properties of gases, however, pose some problems. First, vertical movements
make the contained gases change volume. This means
that the amount of gases inside the swimbladder has to
be adjusted to maintain neutral buoyancy after a change
of depth. Second, gases have to be kept from escaping
the swimbladder despite a pressure gradient that is proportional to depth and therefore steep at great depths
(Lapennas and Schmidt-Nielsen, 1977; Ross, 1979).
Third, the fish will need an organ capable of filling
the swimbladder with gas against the pressure gradient found between the gasses dissolved in blood and
the gasses inside the swimbladder. Gases dissolved in
seawater are at best in equilibrium with sea surface
conditions. The swimbladder is thus like a pressure
balloon, where filling will be slower and reabsorption
of gases faster at greater depths. These two conditions have implications for the vertical behaviour of the
individual.
Because swimbladder adjustments take time, fish
that move vertically will often be at a depth where the
swimbladder volume is too large or too small to give
the fish neutral buoyancy. If the fish cannot lie at the sea
floor, it has to generate lift, up or down, by hydrodynamic means. Bottom-dwelling fish can often be seen
hovering, waving their pectoral fins to create a downward current (Blake, 1979; Alexander, 2003). Fish that
move forward through the water can use their pectoral
fins as hydrofoils (wings), and in addition create lift
with the caudal fin, by other body features, or by tilting. Hydrodynamic lift can be generated fast and can
be altered quickly, but generally requires more energy
than a swimbladder (Alexander, 1990, 2003).

Buoyancy regulation has hitherto not been mechanistically quantified in behavioural models studying the
trade-offs involved in vertical migration. Earlier models have either assumed the cost of vertical migrations
proportional to depth change (e.g. Rosland and Giske,
1994; Strand et al., 2002), assumed no cost (e.g. Clark
and Levy, 1988), and have furthermore not identified
the constraints imposed by a swimbladder. To improve
the ecological realism of such models, this work pieces
together knowledge from three research areas: swimbladder physiology, hydrodynamics of lift, and bioenergetics.
Comparisons between species have sketched the
broad perspective of advantages and disadvantages
with the different means of buoyancy regulation.
Changes in swimbladder volume are constrained by
time and depth, and hydrodynamic lift by the energy
requirements. The model presented here describes the
processes involved in buoyancy control: swimbladder
volume changes, hovering, swimming with fins as hydrofoils and with a tilt angle. These different modes
of buoyancy regulation have different rates, different
energetic costs, and different constraints, and have
been well-studied separately (Alexander, 1971; Blake,
1979; Harden Jones and Scholes, 1985; Vogel, 1994).
By formulating them in a common bioenergetics framework, the trade-offs between the swimbladder and hydrodynamic forces as means of buoyancy regulation
can be compared. The model can answer two lines of
questions: (1) on the shorter time-scale, which types of
behaviour are possible with regard to the physiological
constraints involved, and (2) in the longer run, what
are the energetic costs of the different modes of buoyancy regulation. Insights from this last approach can
be used to interpret field data from free-ranging fish,
and the bioenergetics currency allows comparisons of
costs and benefits of different foraging behaviours to be
studied. By implementing the model presented here as
a submodel in behavioural models, questions into the
adaptive nature of foraging behaviour and other types
of behaviour involving vertical migrations in pelagic
fish can be investigated.
Fish have adapted to a great range of environments,
and the constraints that a swimbladder forces upon
the general physoclist fish will be hard to examine.
To better investigate the models properties, speciesspecific values for Atlantic cod (Gadus morhua) were
used. This is the physoclist species that has been most

E. Strand et al. / Ecological Modelling 185 (2005) 309327

extensively investigated with regard to swimbladder

function (e.g. Tytler and Blaxter, 1973; Harden Jones
and Scholes, 1985; Arnold and Greer Walker, 1992).
Cod are known to perform vertical migrations (e.g.
Brunel, 1965; Beamish, 1966; Metcalfe and Arnold,
1997; God and Michalsen, 2000), but the energetic
cost of this behaviour with regard to variations in buoyancy has been poorly investigated. The model was applied to a time series of vertical positions recorded for
cod by data storage tags (God and Michalsen, 2000)
in order to illustrate the dynamics of the presented
models predictions.

2. Model description
The equations that describe buoyancy control in this
model are intended for recalculation over several timesteps. For every time-step, the following procedure
takes place: (1) the fish depth is used as input; (2) leakage from the swimbladder is calculated based on this
depth; (3) the buoyancy experienced by the fish at the
actual depth is estimated based on the new state of its
swimbladder (change of depth and leakage); (4) maximum rates for secretion and absorption of gases are calculated. The required secretion/absorption takes place
within these limits; (5) the buoyancy not accounted for
by changes in swimbladder volume has to be generated
by hydrodynamic forces, i.e. through increased swimming at the optimal tilt angle, or by hovering; (6) the
metabolic costs of secretion and compensatory swimming are summarised.
2.1. The swimbladder
Physoclist fish have the ability to secrete gas through
a gas gland on the swimbladder wall (Prosser, 1973).
The gas gland produces lactic acid and CO2 , which
lower the pH and increase the concentration of solutes
in the blood. Direct and indirect effects effectuate the
release of haemoglobin-bound oxygen and physically
dissolved gases through the Bohr, Root, and saltingout effects (Jobling, 1995; Schmidt-Nielsen, 1997; Pelster, 2001). In addition, the arterial blood supply flows
through a counter-current vascular arrangement (rete
mirabile) that multiplies blood gas tensions and maintains pH and solute concentrations in the gas gland.
As a result, gas tension in the gas gland may exceed

311

that of arterial blood several-fold, and gases thus diffuse into the pressurised swimbladder (Scholander and
van Dam, 1954; Kuhn et al., 1963; Steen, 1963a).
During ascents, physoclist fish will reabsorb the excess gas inside the swimbladder through a particularly
vascularised area called the oval (Fange, 1953; Steen,
1963b). The rate of absorption is limited, however, and
rapid ascents can thus be dangerous to physoclist fish,
as the swimbladder may expand beyond control or burst
(Harden Jones, 1952; Tytler and Blaxter, 1973).
In this model, leakage and the maximum sustainable rates of secretion and absorption are based on gas
composition with emphasis on oxygen, while the energetic cost of secretion is calculated based on physical work and a biological efficiency factor. Wherever
physically dissolved gases are involved, all gases in
the swimbladder are assumed to have the same physical
properties as oxygen. This approximation can be partly
justified since the next two components, CO2 and N2 ,
have a higher and lower solubility, respectively. Furthermore, other gases (Ar, Ne, He) can be found in the
swimbladder to varying degrees, and the gas composition will hence change in a complex manner resulting
from past vertical behaviour. The equations relating to
haemoglobin-bound oxygen use a partial pressure of
oxygen in the swimbladder that is a constant fraction
of the hydrostatic pressure. Because CO2 has a higher
solubility than O2 , this will tend to underestimate absorption rates during the initiation of absorption (when
CO2 would have been removed faster), but will slightly
overestimate rates after the majority of CO2 has been
removed (which means that N2 would have been more
important for the overall rate of absorption) (Steen,
1963b and references therein). The model can be elaborated to incorporate gases with different physical properties, but at this point such a level of detail was not
found worthwhile. The partial pressure of oxygen and
other gases would then become dynamic, and the model
could thus also shed light on how behavioural decisions
influence the actual gas composition of the swimbladder. Although a full modelling of all gas components
may be possible, it is beyond the scope of this paper.
SI units have been preferred throughout this paper,
although it may seem awkward to measure the volume
of the swimbladder of a small cod in cubic metres. This
makes the equations easier to read, and will thus hopefully enhance understanding of the concepts involved.
See Table 1 for details on all variables.

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

Table 1
Variables and parameters used in the model for buoyancy regulation
Description

Value

Unit

0.050.20

Degrees

mol s1

N
m
m3 s1
J s1
m
N

mol s1
kg
J s1
J s1
mol s1

J s1

P
Ss
Thrust
U; UH
Umax
Vn ; V s
z; zc

Tilt angle
Energy conversion efficiency during swimming
Maximum rate of O2 absorption
Increase in energy expenditure during swimming
Buoyancy force
Body length
Cardiac output
Energy used for gas secretion
Pectoral fin length (at right angle from body)
Lift and drag force, subscript referring to fin, body and tilt
angle ()
Oxygen leakage from swimbladder
Body mass
Metabolic cost of hovering
Additional metabolic cost of extended fins
Maximum O2 that can be secreted into swimbladder; actual
O2 secreted
Standard metabolic rate; total metabolic rate including fin
drag; active metabolic rate (measured metabolism-SMR)
Hydrostatic pressure
Swimbladder surface area
Power produced during swimming
Fish swimming speed; horizontal component
Maximum sustainable swimming speed
Neutral swimbladder volume; current swimbladder volume
Depth; critical depth

1 + (z/10)

atm
m2
N
m s1
BL s1
m3
m

Parameters
;

O2
f ; w

Intercept and slope for allometric function for SMR

Fin beat angle during hovering
Fraction oxygen in secreted gases
Fish tissue density; water density

0.397; 0.828

0.63
1081; 1026

Radians

kg m3

Hb
a/b
Crete ; Coval
Eeff
F (T)
G
g
HGROUND
[L/D]body
O2a
O2sol
P0
R

Fraction of haemoglobin available for O2 binding (in oval)

Length to width ratio of swimbladder
Fraction of cardiac output to rete; to oval
Energy conversion efficiency during secretion
Temperature function for SMR
Oxygen conductance
Gravitation constant
Energy saving during hovering due to ground effect
The lift-to-drag coefficient for body
O2 content of arterial blood by volume
Solubility of O2
Pressure at surface
Universal gas constant

0.15
10
0.10; 0.25
0.10
0.502 at 5 C
1.5 109
9.81
1
0.75
0.10
0.04
1
8.206 105
8.3144

m3 O2 m2 atm1 s1
m s2

m3 O2 m3 blood1 atm1
atm
m3 atm mol1 K1
J mol1 K1

Reff
T

Rete efficiency
Ambient temperature

0.20
278.15

Variables

Absmax
Act
B
BL
Cout
Esec
FL
L; D
Leakage
M
MRHOVER
MRPECT
Secmax ; Sec
SMR; TMR; AMR

Species-specific values refer to Atlantic cod (Gadus morhua). Variables and parameters without dimension are denoted in the unit column.

E. Strand et al. / Ecological Modelling 185 (2005) 309327

2.2. Neutral buoyancy

which oxygen leaks from the swimbladder (Leakage;

mol s1 ) is:

A submerged fish has neutral buoyancy when it displaces a volume of water with a mass equal to its body
mass (Archimedes principle). The volume of a swimbladder giving neutral buoyancy (Vn ; m3 ) to a fish with
body mass M (kg) can then be calculated given the density of the fish tissue (f ; kg m3 ) and the density of
water (w ; kg m3 ):
Vn =

M(1 (w /f ))
w

(1)

both w and f can be modelled as variables to reflect heterogenic environments and ontogenetic and
seasonal changes for the particular species (discussed
in e.g. Ona, 1990).
The amount of gas (mol) in the swimbladder was
calculated using Boyles law (Harden Jones, 1951;
Alexander, 1959). If the actual swimbladder volume
(Vs ; m3 ) differs from Vn , the fish will experience positive or negative buoyancy force (B; N):
B = (Vs Vn )w g

313

(2)

where g is the gravitation constant (9.81 m s2 ).

2.3. Swimbladder leakage
A swimbladder will need constant refilling due to
diffusion into surrounding tissues (Denton et al., 1972;
Lapennas and Schmidt-Nielsen, 1977; Ross, 1979).
Oxygen diffusion is dependent on three variables: the
oxygen permeability of the swimbladder wall, which
again is dependent on its species-specific guanine and
lipid content (Denton et al., 1972; Wittenberg et al.,
1980); the swimbladder surface area (Ss ; m2 ); and the
pressure gradient between the swimbladder and surrounding tissues (P P0 ; atm). The swimbladder of a
general teleost is assumed to be formed as a prolate
(cigar-shaped) ellipsoid with polar radius a (m) and
equatorial radius b (m). The swimbladder surface is
calculated based on the current swimbladder volume
(Vs ) and a and b (a = ((Vs 3(a/b)2 )/(4))1/3 when the
ratio a/b is known):



(a/b) arcsin(e)
Ss = 2b2 1 +
(3)
e
where e (dimensionless)
is the eccentricity of the el
lipse given by e = (1 b2 /a2 ). Hence, the rate at

Leakage =

GSs (P P0 )
RT

(4)

where G (m3 O2 m2 atm1 s1 ) is the oxygen conductance of the swimbladder wall, R (m3 atm mol1 K1 )
the universal gas constant, and T (K) the temperature
in Kelvin.
2.4. Secretion
The equations for gas secretion are based on work by
Harden Jones and Scholes (1985). It is assumed that the
diffusion barrier between the gas gland and the swimbladder is so little that the rate-limiting step is the transport of oxygen and multiplication of partial pressures
in the rete and the gas gland. As a consequence, secretion will be independent of depth. The model calculates
the maximum rate of secretion (Secmax ; mol s1 ), as a
function of cardiac output (Cout ; m3 s1 ), the fraction of
Cout diverted to the rete (Crete ; dimensionless) (Pelster
and Scheid, 1992), the volume fraction of O2 in arterial
blood (O2a ; dimensionless) measured at P0 (1 atm), and
an efficiency factor of the rete (Reff ; dimensionless):
Secmax =

Cout Crete O2a Reff P0

RTO2

(5)

where O2 is the fraction of oxygen in the secreted

gases. It is likely that both Cout and Crete vary in a complex fashion. At high exercise levels, it is likely that
the rete experiences a reduction in blood flow as the
exercising muscles are given priority. Similarly, at low
activity levels, it is possible that the fish can increase
Cout , and thus blood flow to the rete, when it needs
to speed up absorption or secretion. Therefore, a static
Cout estimated for a typical cruising speed combined
with a static Crete as the maximum measured value will
give a good approximation of maximum blood flow and
thus maximum secretion rate.
The minimal amount of work (W; J) required to
isothermally compress (i.e. at constant temperature)
one mol of gas at temperature T from pressure P1 to
pressure P2 is (Glasstone and Lewis, 1964):


P2
(6)
W = RT ln
P1

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

It is further necessary to divide the minimum energy with an efficiency factor for converting biological
chemical energy into mechanical energy (Eeff , dimensionless). Eeff includes the effects and energetic costs
for the Bohr, Root, and salting-out effects, production
of lactate, and the pentose-phosphate pathway (Pelster
et al., 1989, 1994). If these effects were to be modelled explicitly, it would be necessary to know the cost
and contribution of each of these effects. A precise set
of equations to describe these processes thus requires
further experimental research; in this model the focus
is set on the overall energetic cost of secretion. Esec
(J s1 ) is thus the required energy to secrete the gases:


P
1
Esec = Sec RT ln
(7)
Eeff
P0
where P is the hydrostatic pressure and P0 the combined partial pressures of the gases in arterial blood,
assumed constant (1 atm). Sec is the amount of gases
secreted and always less than or equal to Secmax . The
depth at which the leakage rate equals the maximum
gas secretion rate is termed the critical depth (zc ; m),
and was calculated by finding the pressure at which
leakage from Eq. (4) equals maximum secretion from
Eq. (5) (P = l + z/10):
Secmax RT
(8)
zc = 10
GSs
2.5. Absorption
Physoclist fish have a particular area on the swimbladder wall called the oval, which is specialised for
gas absorption (Fange, 1953; Steen, 1963b). There are
three major variables that influence the rate of oxygen
absorption (Steen, 1963b). First, only the fraction of
the cardiac output that flows through the oval (Coval ;
dimensionless) can absorb oxygen. Second, the pressure gradient between the swimbladder and the arterial
blood (in this model calculated as P P0 ) determines
the amount of gas that can be physically dissolved.
Third, available oxygen-binding sites on haemoglobin
can transport additional oxygen. By adopting the
method of Harden Jones and Scholes (1985), the maximum oxygen absorption rates (Absmax ; mol s1 ) can
be calculated as:


Cout Coval P0 O2sol (P P0 )
Absmax =
+ O2a Hb
RT
O2
(9)

where O2sol the solubility of oxygen (m3 O2 m3

blood atm1 ) and Hb is the fraction of available
haemoglobin binding sites (dimensionless). The O2 includes the other gases that follow physically dissolved
oxygen.
2.6. Hydrodynamic lift
When neutral buoyancy cannot be achieved by the
swimbladder alone, lift (up or down) has to be created
by hydrodynamic forces in order to avoid sinking or
floating. Experimental studies have shown that large
cod, by using their pectoral fins as hydrofoils while
swimming freely, can compensate for 7090% of the
lift from the swimbladder (Ona, 1990). This model considers four distinct methods to create hydrodynamic
lift: hovering without moving through the water, body
lift, changing the tilt angle, and using the pectoral fins
as hydrofoils. Hovering requires that the fish is stationary and cannot be combined with the other methods
for hydrodynamic lift. The last three methods require
that swimming speed and tilt angle are calculated simultaneously to find the most energy-efficient way to
produce the required lift. An overview over the hydrodynamic forces considered is shown in Fig. 1.
The energetic cost of lift production has to be added
to the standard metabolic rate SMR (J s1 ). The total
metabolic rate (TMR; J s1 ) will then be either:
TMR = SMR + MRHOVER + Esec

(10a)
(J s1 )

if the fish is hovering, and where MRHOVER

the metabolic cost of waving the pectoral fins; or:
TMR = SMR + AMR + MRPECT + Esec

is

(10b)

if the fish is swimming. AMR (J s1 ) is the energetic

cost of swimming and MRPECT (J s1 ) is the additional
cost of lift production via the pectoral fins. AMR is
equivalent to measured metabolic rate during swimming minus the standard metabolic rate. For a fish that
beats a pair of fins of length FL (m) through an angle
to create a force equal to the buoyancy, the metabolic
cost will be (Alexander, 2003):

|B|3
MRHOVER = HGROUND
(11)
2WFL2
HGROUND (dimensionless) is a factor that includes
the energetic saving that can be obtained if hovering

E. Strand et al. / Ecological Modelling 185 (2005) 309327

315

part of the thrust vector is directed downward, and the

horizontal velocity, which is the fish speed through
the water that can generate other types of lift, will be
UH = cos U. A closer inspection of available literature
on the metabolic cost of swimming revealed that swimming efficiency increased with swimming speed (e.g.
Sepulveda and Dickson, 2000; Dickson et al., 2002;
Nauen and Lauder, 2002). It was necessary to introduce the factor (dimensionless), which is the biological efficiency of converting chemical energy to a
propelling force. It is here modelled as a function of
U2 (reasons for the parameter and its mathematical
formulation are given in Section 4):





U 2
max min
= min +
(14)
2
BL
Umax

Fig. 1. Schematic drawing of the forces acting on a fish with swimbladder. (a) The forces acting on a negatively buoyant fish swimming
horizontally. Thrust will equal drag at constant velocity. Lift is created by using the pectoral fins as hydrofoils (Lfin ) and by the general
body surface (Lbody ). (b) When the fish is tilting, the thrust vector
can also produce lift (L ). This will also affect the efficiency with
which the pectoral fins and the body can create lift.

takes place close to the bottom (less than the length of

the pectoral fins above solid substrate; (Blake, 1979).
HGROUND takes a value <1 when the fish is negatively
buoyant and close to the bottom and 1 for all other situations. Blake (1979) calculated potential savings in the
range 3060% for the mandarin fish Synchropus picturatus. We have assumed that hovering is a potential
option only for negatively buoyant fish.
The fish can also change its tilt angle . The Thrust
(N) will then have a vertical component, which will
give a lift L (N):
L = sin Thrust

(12)

To find the thrust vector, we use the relationship

power = force velocity. Since power here is equal to
the metabolic rate associated with swimming, we have:
Thrust =

AMR
U

(13)

where U (m/s) is the swimming speed that the fish

would have had if neutrally buoyant and swimming
with the same metabolic cost. When the fish is tilting,

where min and max are minimum and maximum values for , respectively, and Umax is the maximum sustained swimming speed measured in BL s1 . Typically,
would scale between min = 0.05 and max = 0.20.
Defining in this way preserves Dbody as a function of U22.5 , and lets scale with body size in accordance with the biological interpretation. For most
species Umax decreases with body size and increases
with temperature.
Given that the fish maintains a constant speed, the
horizontal component of the thrust vector will be equal
to the body drag Dbody (N):
Dbody = cos Thrust

(15)

Many fish utilize also the body drag to produce

lift, e.g. through having a dorsal curvature that gives
the overall body a wing shape, or by specifically designed appendages. Holding the lift from the pectoral
fins aside, we define body lift Lbody (N) as the nonreversible (always working only upward) lift from the
body:
 
L
Lbody =
Dbody cos
(16)
D body
L
is a positive lift-to-drag coefficient for
where D
body
the body as a whole. A perfectly designed fin can have
lift-to-drag coefficients up to 5 (Alexander, 1971), but
the value for the whole body will for most fish be substantially lower. Note that since Dbody is always positive, Lbody will also be a non-negative value.

316

E. Strand et al. / Ecological Modelling 185 (2005) 309327

The pectoral fins can be extended as hydrofoils,

which will increase the drag but also be very efficient
at producing lift. We assume that the pectoral fins become less efficient at producing lift when the tilt angle
increases; Lfin /cos is therefore used in the equation.
The extra energy required to produce Lfin (N) lift is then
(Alexander, 1990, 2003):
MRPECT =

(Lfin / cos )2
w UH FL2

(17)

The number 4 in the denominator in Alexanders

original equation is cancelled by our use of fin length
FL , which is only half the span of the pectoral fin hydrofoil and when squared produces a 4 also in the numerator.
We now assert that the vertical forces have to sum
to zero:
B = L + Lbody + Lfin

(18)

The best combination of tilt angle and swimming

speed U can now be iterated from the set of equations
by minimizing the sum of AMR and MRPECT . The
resulting cost of swimming to create hydrodynamic lift
can then be compared to the energetic cost of hovering
to see which option is favourable in energetic terms.
2.7. An example: Atlantic cod
To test this description of buoyancy control, the
model was parameterised for Atlantic cod (G. morhua).
For some parameters, experimental values had not been
obtained for cod, and we were forced to use values
from other species. In a model as complex as this one,
there will necessarily be biological parameters not yet
experimentally determined. For this reason, emphasis was put on matching the overall output from the
models different components with data where available, and uncertain parameters were tuned against experimental studies on cod swimbladder dynamics and
swimming physiology (e.g. Tytler and Blaxter, 1973;
Harden Jones and Scholes, 1985; Sepulveda and Dickson, 2000). To help visualize the sensitivity of the predicted output from the model, many of the results are
plotted for fish of various sizes and over a wide range
of swimbladder volumes.
A value of 1081 kg m3 was used for cod tissue density (Harden Jones and Scholes, 1985). Based on Xray pictures of cod (Clay and Horne, 1994), the length

to width ratio (the a to b ratio in Eq. (3)) was estimated to be 10. Scholander (1956) found that O2 made
up on average 63% of the secreted gases in cod, thus
O2 = 0.63. The energy converting efficiency during
secretion was set to Eeff = 0.10 (Alexander, 1971). The
oxygen content of arterial fish blood was set to 10% by
volume (O2a = 0.10, Prosser, 1973; Harden Jones and
Scholes, 1985). Steen (1963a) obtained experimentally
a rete efficiency of 20% in the eel (Anguilla anguilla),
thus Reff = 0.20. These parameters describe secretion in
accordance with the experiments in Harden Jones and
Scholes (1985).
The total metabolic cost (TMR; Eq. (10b)) was
calculated based on a general bioenergetic model
by Hewett and Johnson (1992) with cod parameters
(Hansson et al., 1996):
SMR = M F (T )

(19a)

AMR = SMR Act

(19b)

Act =

3.2U 1.5
BL

(19c)

where M is a weight dependent and F(T) a temperature dependent function of metabolism with = 0.397,
= 0.828, and F(T) = 0.502 at 5 C (see Hansson et al.,
1996 for details). Act (dimensionless) is the incremental cost of activity and is estimated based on measurements of oxygen consumption during swimming (U)
for cod in the range 0.241.91 kg (expressed on the
form used in Ware, 1978; Schurmann and Steffensen,
1997; Webber et al., 1998; Reidy et al., 2000).
Cardiac output (Cout , m3 s1 ) based on data from
Webber et al. (1998) was calculated as a function of
body mass and the metabolic rate corresponding to a
cruising speed of 0.4 BL s1 :
Cout = 9.07 107 TMR 3.79 108 M

(20)

Pectoral fin length (FL ) was calculated from body

length (BL) using a relationship obtained for cod ranging from 10 to 105 cm (based on unpublished data from
A.G.V. Salvanes; n = 400, R2 = 0.98):
FL = 0.1374BL + 0.0039

(21)

Following Alexander (2003), the angle through

which the fin beats when hovering was set to = radians. Maximum sustainable swimming speed (Umax ;
BL s1 ) was modelled to fall from 1.8 BL s1 in 0.2 kg

E. Strand et al. / Ecological Modelling 185 (2005) 309327

317

cod and stabilise at 1.2 BL s1 in cod > 3 kg (based on

data from Schurmann and Steffensen, 1997; Webber et
al., 1998; Reidy et al., 2000):
Umax = 0.8eM + 1.2

(22)

The parameters G (the oxygen conductance of the

swimbladder wall), Crete , and Coval (the proportion
of cardiac output that can be directed to the rete
and the oval, respectively) have to our knowledge
not been measured for cod. Harden Jones and Scholes (1985) measured rates of absorption and secretion in cod, and these parameters were chosen to
match their experimental results. The blood flow to the
oval (Coval ) was measured in anaesthetized eel (Anguilla vulgaris) by Steen (1963b) and found to be
in the range 628%. Crete has to our knowledge not
been measured. Since the rete with its counter-current
vascular structure is much more elaborate than the
oval, we used Coval = 0.25 and Crete = 0.10, two values
that provided good fit with the experimental data on
cod from Harden Jones and Scholes (1985). Lapennas
and Schmidt-Nielsen (1977) measured oxygen conductance G between 1.5 109 and 1.5 108 m3
O2 m2 atm1 s1 in the deep-dwelling Conger eel
(Conger oceanicus) and five teleosts utilising shallower habitats compared to cod. A value in the lower
range, G = 1.5 109 , was chosen so that a 2-kg cod
would have a critical depth zc 533 m. The models
predictions of net secretion rates and critical depths
are sensitive to the numerical value of G; any choice
of G should therefore be accompanied by comparisons
of critical depths with the species vertical distribution. Cod is regularly found down to depths of 400 m
(God and Michalsen, 2000), and because secretion
(by volume) is very slow close to the critical depth,
our choice of G implies that the cod over its entire vertical range has a swimbladder that responds to depth
change within reasonable time (Fig. 2a). Data on ontogenetic changes in the gas conductivity of swimbladder
wall tissue has, to our knowledge, not been published.
Gas conductivity was therefore assumed constant in
this model.
L
We assumed D
= 0.75, which is the converbody
sion of drag over the fish body to a vertical lift component (discussed in Vogel, 1994, pp. 239240); the
parameter has to our knowledge not been determined
for fish). This included lift produced by the overall body

Fig. 2. Swimbladder dynamics as a function of depth in a model

parameterised for cod Gadus morhua. (a) Absolute leakage (dotted
line), secretion (dashed line), and absorption (solid line) as a function of depth, expressed in (mol kg1 s1 ). The grey area is the
difference between leakage and maximum secretion and is thus the
maximum net secretion possible at that depth, (b) Net secretion and
absorption, both including the effects of leakage, measured in volume (l kg1 s1 ). The calculations were made for a 2-kg Atlantic
cod. Note the log x-axes.

surface and body shape, and resulted in a slight asymmetry in the energetic cost between creating positive
and negative lift.
To our knowledge, no study has ever combined measures of different aspects of buoyancy regulation to a
degree that can be used as a set of independent data
to validate the model described above. That would require simultaneous measures of gas rates, buoyancy,
swimming speed and mode, and metabolic rate. Rather,

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

swimbladder dynamics and hydrodynamic lift generation has to be tested separately against experimental
datasets, and the combination of the two in a bioenergetic framework can at present only be shown, not
tested. To compensate this, we have tried to use parameter values from published experiments and strived
to make our thoughts and assumptions as clear to the
reader as possible. We have also taken two approaches
to demonstrating the benefits from combining swimbladder dynamics and hydrodynamic lift generation.
First, we show estimates for the energetic cost of buoyancy control for a series of constructed patterns for diel
vertical migration for a 2-kg cod. Each migration pattern was simulated for 6 days to stabilize, and results
were shown for the last 24-h period only. Second, we
visualise the model using 12 months of data on vertical positions collected from a 3-kg cod carrying a data
storage tag (resolution 2 h, interpolated to time-steps of
15 min, from God and Michalsen, 2000). The cod was
tagged on the 21 March 1996. To assure that any possible handling wounds would have healed, three weeks,
starting at 22 October 1996, were selected for visualisation.

3. Results
Several authors have studied different modes of
buoyancy regulation (e.g. Steen, 1963a; Alexander,
1972; Harden Jones and Scholes, 1985; Vogel, 1994).
The results presented here provide the basics of the
different modes, but focus on the link between swimbladder dynamics and hydrodynamics made possible
in our paper by the common bioenergetics approach. It
is in the linking of the different modes of buoyancy regulation in a common currency that our work transcends
earlier work and creates a basis for future behavioural
models and field data interpretation.
3.1. Swimbladder dynamics
The swimbladder is subject to the physical laws for
gases, which make swimbladder dynamics dependent
on both depth and body size. To clarify the picture, we
will describe how rates, in mol s1 , vary with depth,
and then focus on how this is translated into volume
changes and affect the behavioural repertoire.

The processes that describe leakage and absorption

of gases from the swimbladder depend on the difference in partial pressure between the swimbladder (at
hydrostatic pressure) and the surrounding tissues including blood (in equilibrium with sea surface conditions at best). As this pressure difference increases
with depth, the rates for these two processes will also
increase (Fig. 2a). The absolute gas secretion rate is, on
the other hand, unaffected by depth (Fig. 2a). Consequently, the net rate of gas secretion, which is how fast
the swimbladder can be filled, decreases with depth (the
shaded area in Fig. 2a). Note that these rates are maximum rates, and we assume full regulatory flexibility
within these limits.
The pattern of volume changes is different from secretion and absorption rates, due to the increasing hydrostatic pressure with depth (Fig. 2b). Although more
gas molecules (measured in mol) can be absorbed with
depth, the volume that can be absorbed is almost independent of depth except for slow changes close to
the surface. Overall, the volume that can be absorbed
is much larger than the volume that can be secreted
per unit time (the axis in Fig. 2b is logarithmic; absorption volume is 1010,000 times larger than the
secretion volume depending on depth). Maximum net
secreted volume declines rapidly with depth and approaches zero where leakage and secretion rate cancel
each other. This asymmetry between absorption and
secretion means that fish will more often be negatively
than positively buoyant (noted by Alexander, 1966;
Tytler and Blaxter, 1973; Arnold and Greer Walker,
1992). In addition, filling the swimbladder is radically
slower at greater depths, which will affect the costs and
benefits of vertical behaviour.
Harden Jones and Scholes (1985) present to our
knowledge the best experimental data set on absorption and secretion in cod. We have carefully chosen the
parameter values of Crete and Coval so that the swimbladder dynamics of our model match their data within
10% over the range of depths included in their study.
Our estimates are also very similar to those obtained
experimentally by Tytler and Blaxter (1973). Because
the surface:volume ratio decreases with increasing size,
a larger fish will have a relatively lower gas leakage
across the swimbladder wall. As a result, critical depth
increases with body size (Fig. 3).
Energy is required to pressurise gases in the
blood to fill the swimbladder. When gas secretion

E. Strand et al. / Ecological Modelling 185 (2005) 309327

319

Fig. 3. Size dependence of critical depth and leakage across the

swimbladder wall. The surface-to-volume ratio of the swimbladder
changes as a cod grows in size. As an effect, the relative amount of
gas leaking across the swimbladder wall decreases with body size
(grey line). Critical depth, i.e. the depth at which maximum secretion
equals gas leakage, will thus increase with body size (black line).

is at its maximum, the estimated energetic cost is

0.0017 J kg1 s1 . This corresponds to 1.0% of the
standard metabolism and is, as will be shown below,
close to negligible compared to the energy required for
swimming.
3.2. Hydrodynamic lift
If neutral buoyancy can not be achieved through the
swimbladder alone, the fish must depend on hydrodynamic lift to maintain its position in the water column.
The present model assumes that lift is produced either
by hovering, or by swimming at the optimal tilt angle, which would combine pectoral fin lift, body lift,
and lift from the tilted thrust vector. Lift created by
hydrodynamic forces is independent of depth. We will
present results for fish of varying body mass, and for
lift production corresponding to swimbladder volumes
ranging from 100% (empty swimbladder) to +100%
(double size) of the optimal volume. We will first focus
on hydrodynamic lift created during swimming, before
we turn to hovering as an alternative and compare the
two.
The more the swimbladder volume deviates from the
optimal volume, the higher was the estimated compensatory swimming speed (Fig. 4a). The compensatory
swimming speed also increased with fish size when
measured in m s1 , but when measured in BL s1 it did
not vary with body mass. Each half of Fig. 4a had the

Fig. 4. Properties of hydrodynamic lift production when the swimbladder volume deviates from optimal. The left-to-right axis is the
swimbladder volume, where 0% corresponds to the optimal volume
that would have resulted in neutral buoyancy. Negative buoyancy
(sinking) is to the left; positive buoyancy (floating) to the right. Fish
size (kg) increases from 0.2 kg in front to 5.0 kg in the back. (a) Compensatory swimming speed, expressed in body lengths per second
(BL s1 ). (b) The values taken by the energy conversion efficiency
between the fish oxygen consumption and the physical work required to overcome drag. increases with increasing swimming
speeds up to maximum sustainable swimming speed, where it would
reach a maximum of 0.20. (c) The optimal tilt angle at different levels
of buoyancy and fish size. Panels (a) and (b) assume that the fish was
swimming at the optimal tilt angle.

expected concave-up shape: the deviation in swimbladder volume is proportional to the required lift, which is
proportional to drag, which again is a function of U23 .
This was achieved by the energy conversion efficiency

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

(Fig. 4b), which scales with swimming speed from

0.05 (at zero swimming speed) to a maximum value of
0.20 (at the maximum swimming speed; see Section 4
for details).
Close to neutral buoyancy, fish will have a low energy conversion efficiency . They will therefore use
relatively more energy for swimming at the speed that
creates sufficient drag for lift production, which in turn

will favour a steeper tilt angle (Fig. 4c). The optimal

tilt angle increased also for small fish. This is because
smaller fish have a higher maximum sustainable swimming speed (Eq. (22)) and will hence achieve a relatively lower energy conversion efficiency . For most
combinations of size and buoyancy, the optimal tilt angle was found to be around 7 for both positive and
negative buoyancy.
For lift produced by compensatory swimming, the
energy expenditure, measured per kg body mass, was
strongly dependent on the experienced buoyancy, but
showed little variation between fish of different size
(Fig. 5a). The asymmetry between negative (left half)
and positive (right half) buoyancy seen in Fig. 5a is
due to body lift. Body lift will always work towards
the surface due to the shape of the fish, irrespective
of the buoyancy force experienced by the fish. Whenever the fish is negatively buoyant, body lift will reduce
compensatory swimming speeds and thus also energy
requirements, while the opposite effect takes place during positive buoyancy.
The energetic cost of hovering is shown in Fig. 5b.
In our model, hovering is only possible when the fish
is negatively buoyant. The energetic cost of hovering
rose sharply with the degree of underflotation and with
increasing body size. Because the energy consumption during compensatory swimming was a concavedown function and that for hovering concave-up, hovering was energetically preferential when the fish was
only slightly negatively buoyant (Fig. 5c). Hovering
was also more often the best option for smaller fish.
Small fish, experiencing close to neutrally buoyancy,
gain most from tilting compared to fish orientated hor-

Fig. 5. Energy consumption for different modes of hydrodynamic lift

production. The left-to-right axis is the swimbladder volume, where
0% corresponds to the optimal volume that would have resulted in
neutral buoyancy. Negative buoyancy (sinking) is to the left; positive
buoyancy (floating) to the right. Fish size (kg) increases from 0.2 kg
in front to 5.0 kg in the back. The calculations assume that the fish
were swimming at the optimal tilt angle. The graphs show energy
expenditure (J kg1 s1 ) to produce the required lift by means of (a)
hydrodynamic lift by swimming with the pectoral fins extended, (b)
standing still hovering, and (c) the most energy-efficient combination
of pectoral fins and hovering. The area where hovering is beneficial
is indicated by the thick black line. Panel (d) shows how much energy
fish gain from applying the optimal tilt angle (see Fig. 4c) compared
to orientating the body horizontally (tilt angle = 0 ). See text for details.

E. Strand et al. / Ecological Modelling 185 (2005) 309327

321

izontally (in percentage change between tilting and

non-tilting) (Fig. 5d). Larger fish gain relatively less
than small fish independent of buoyancy level. However, the absolute amount of energy saved by tilting
(kJ kg1 s1 ) increases for all size classes with both
decreasing and increasing buoyancy.
3.3. Ecological implications
Hydrodynamic forces stemming from swimming
and lift from the swimbladder often complement each
other in producing lift; the swimbladder being slow
to adjust but energetically cheap to operate while hydrodynamic forces have the opposite properties. To
show how these two modes of lift production work together, we show the estimated energetic cost for various
vertical migration patterns in Fig. 6. The example assumes that cod stayed at 200 m depth during daytime
and migrated to shallower waters during the night to
feed (this behaviour is representative for cod, see e.g.
God and Michalsen, 2000). The vertical movement
was set to take always 1 h, so that 11 h were spent at
the top and the bottom of the vertical range (examples are shown in Fig. 6a). Because gases are absorbed
much faster than they are secreted, the cod was close
to neutrally buoyant at the top of the vertical range.
At the daytime depth, cod became progressively more
negatively buoyant as the vertical migration distance increased (Fig. 6b). Consequently, hydrodynamic forces
had to compensate for negative buoyancy through increased swimming (Fig. 6b), and the energetic cost
increased rapidly with increasing vertical migration
distance (Fig. 6c). During night, fish that stay closer
to the surface experience a lower leakage and hence
cheaper maintenance of the optimal swimbladder volume, which is the reason that the energetic cost fall
with migration distance (Fig. 6c).
3.4. Application to eld data
The model predictions were further explored by applying it to a set of observed vertical positions of an individual cod recorded over one year using a data storage
tag (God and Michalsen, 2000, Fig. 7a). Only a subset
of three weeks starting 22 November 1996 is presented.
It was assumed that the fish had neutral buoyancy at
the start of the period and the first simulated day is
not shown to allow the simulated swimbladder volume

Fig. 6. A constructed example of diel vertical migration in cod and

the corresponding predictions of swimbladder volume, swimming
speed and energetic cost from a model paramterised for cod Gadus
morhua. (a) Examples of constructed diel vertical migration patterns
for which buoyancy regulation were simulated for a 2-kg cod. The
pattern was simulated for 6 days to stabilise; only the results for the
last 24-h period are shown, (b) Mean swimbladder volume and compensatory swimming speed to create the required lift at the daytime
depth as a function of the vertical migration distance. At the top of
the vertical range, swimming speed was close to zero and the swimbladder volume virtually optimal, (c) The energetic cost of buoyancy
regulation separated by the periods spent at the bottom (day) and top
(night) of the vertical migration profile.

to stabilize. The model was not sensitive to the choice

of initial swimbladder volume. Estimated swimbladder
volumes were between 40 and 0% deviation from optimal volume (Fig. 7b). Calculated energy expenditure,

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

Fig. 7. (a) The observed vertical position of one Atlantic cod over a period of three weeks (data from God and Michalsen, 2000). (b) The models
prediction of the cods experienced swimbladder volume expressed in percent deviation from the optimal swimbladder volume that would have
given neutral buoyancy. The cod was assumed to be neutral at time 0 and the first day is not shown to allow the swimbladder volume to stabilise.
The horizontal line is optimal swimbladder volume. (c) The corresponding energy consumption (J kg1 s1 ) due to standard metabolic rate, the
cost of gas secretion, and activity metabolism caused by compensatory swimming speed when the swimbladder volume deviated from optimal.
The standard metabolic rate (SMR) is identifiable as the baseline (swimbladder volume optimal and thus no need for compensatory swimming).
(d) The black bars indicate when the model predicted that hovering would have been an energetically favourable option.

including secretion and compensatory swimming, is

shown in Fig. 7c. The standard metabolic rate (SMR)
is recognisable as the baseline for energy expenditure.
Late on day 17, the cod went down to around 100 m and
stayed there for several days with only short vertical
migrations to shallower depths. The model estimated
that secretion slowly filled the swimbladder, and predicted decreasing compensatory swimming speeds that
would lead to a steady decrease in energy expenditure.
After approximately 2 days, the swimbladder had attained optimal volume. Hovering was not enabled in
this simulation, but the energetic cost of hovering was
calculated for comparison. The black bars in Fig. 7d in-

dicate when the model predicted that hovering would

have been energetically favourable. As expected, hovering was only favourable when the fish was close to
neutrally buoyant; in total 50% of the time.

4. Discussion
The presentation of this model is based on parameter
values for cod. In a strict sense, the results apply only to
cod. However, throughout this discussion of buoyancy
regulation we try to establish a wider perspective, aiming at making general points with validity for a broad

E. Strand et al. / Ecological Modelling 185 (2005) 309327

range of fish species that have physoclist swimbladders.

More precise predictions will require that the model is
re-parameterised for the relevant fish species. It should
be possible to apply an adjusted version of the model
to some physostome fish by allowing the fish to expel
air if it becomes positively buoyant. It is also unclear
to what extent physostome fish are capable of secreting
gas (Moyle and Cech, 1988; Nttestad, 1998).
4.1. The swimbladder
There are complex changes in the available behavioural repertoire of physoclist fishes with increasing depth. For example, frequent vertical movements
will lead to negative buoyancy because absorption is
faster than secretion, an effect that is amplified on
greater depths. This is mainly due to the fact that net
gas secretion is reduced while gas absorption is faster
with increasing depth. Ontogenetic differences also impact swimbladder characteristics in many ways. During
growth, the surface to volume ratio of the swimbladder decreases. This reduces the relative gas leakage
from the swimbladder, giving larger fish a comparative
advantage at greater depths. To what extent such an
ontogenetic shift is involved in shaping the vertical positioning strategies of different-sized fish is, however,
difficult to estimate as so many other important aspects
of evolution can affect behaviour (e.g. predation risk,
food accessibility).
Note also that the rates calculated are maximum
rates and that regulation takes place within the calculated limits, analogous to nervous control with physiological constraints. The swimbladder wall is provided
with stretch receptors (Qutob, 1962) and innervated by
the autonomous nerve system (Wahlqvist, 1985; Schwerte et al., 1997). Although this would imply that fish
are unable to deliberately plan whether or not to secrete or absorb gas, it would instead allow fish to autonomously and continuously adjust their swimbladder
volume towards neutral buoyancy with great flexibility
within the calculated limits.
4.2. Negative versus positive buoyancy
First, it would be instructive to establish to what
extent over- or underflotation occur in nature. Current interpretations of empirical data conclude that cod
stays neutral near the top of its vertical range and be-

323

comes progressively more negatively buoyant at greater

depths (Alexander, 1971; Harden Jones, 1981; Arnold
and Greer Walker, 1992; God and Michalsen, 2000).
This tendency towards negative buoyancy was also evident when the model was applied to constructed diel
vertical migration patterns and field data. Calculations
made on the observed behaviour from the tagged cod
indicated that most of the time was spent with a swimbladder volume between 40 and 0% deviation from
the optimal volume, and the cod was never significantly positively buoyant. With this in mind, our focus
has been to model situations close to neutral buoyancy
and with underflotation up to 40% as realistically
as possible; the model thus sketches a coarser landscape of energy usage for the less used behaviours.
The model also presupposes a physiologically intact
swimbladder in all situations. If the swimbladders
functionality is compromised, e.g. by rupture during
rapid ascents, certain limitations must be defined in the
model.
A 2-kg cod that swims at a speed of 0.25 BL s1 ,
which is the average swimming speed measured in freeranging cod (due to e.g. food search, horizontal migrations) (Lkkeborg, 1998), would, without increasing
its energy budget, be able to freely deviate within 89
and 106% of optimal swimbladder volume. Adapted to
100 m, this means that moving between 93 and 114 m
would be without additional energetic costs. For a cod
adapted to 300 m, this range would extend from 282 to
338 m.
Buoyancy can be both positive and negative, and
creating a lift to overcome it may turn out to be different depending on whether the force has to be created up
or down. Three aspects suggest that there is an asymmetry: (1) gas absorption is much faster than gas secretion.
A fish is therefore likely to spend much more time negatively than positively buoyant, and should thus be most
efficient at counteracting negative buoyancy. (2) The
lift generated by a wing that moves through a medium
is dependent among other factors on wing shape, surface area, and angle of attack (Vogel, 1994). Although
the pectoral fins of cod are highly manoeuvrable in all
directions, the posterior part of the fin base is positioned more ventrally than the anterior fin-base: this
gives the fins a positive angle of attack. (3) Dorsal
curvature and flattened fish bodies may also provide
lift merely by moving forward through thewater. This
L
asymmetry is included in the parameter D
, which
body

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

in a broad interpretation includes the effects of point

2 and 3 above. As a result, it is energetically cheaper
to produce positive lift, which is the common situation
since fish are most often negatively buoyant.

elasticity can be brought into play by the undulating

fish body. would typically be higher in fish species
well-adapted to prolonged or fast swimming.
4.4. Tilt angle

4.3. Energy conversion

There is a paradox in the way active metabolic
rate scales with swimming speed that became apparent during the work trying to solve the equations for
drag involved in this paper. Body drag is most likely
to be proportional to U1.52.0 (Vogel, 1994). Power is
force velocity, which means that active metabolic
rate (AMR; J s1 ) required to overcome body drag
at a given swimming speed, should be proportional
to Dbody U, i.e. proportional to U2.53.0 . Paradoxically, measures of metabolic rate at increasing swimming speeds show that metabolic rate is proportional to
U1.01.5 , not U2.53.0 (Schurmann and Steffensen, 1997;
Webber et al., 1998; Reidy et al., 2000; Sepulveda and
Dickson, 2000). This suggests that fish are more efficient in converting chemical energy into physical work
at higher swimming speeds.
Digital particle image velocimetry can precisely
measure the force exerted on water, and has recently
been applied on swimming fish (e.g. Drucker and
Lauder, 1999). For chub mackerel Scomber japonicus
swimming at constant speed in a flow tunnel, thrust
was found to be a function of U2.5 (Nauen and Lauder,
2002). Metabolic rate should then be proportional to
U3.5 . However, a regression on measurements of active metabolic rate in another study on chub mackerel revealed that metabolic rate was a function of
U1.1 (Sepulveda and Dickson, 2000; Dickson et al.,
2002). A closer look on the data reveal that the ratio between physical work per time (Nauen and
Lauder, 2002) and metabolic rate (Sepulveda and Dickson, 2000) increased from 0.05 at 1.2 BL s1 to 0.20
at 2.2 BL s1 . Such an increased efficiency can explain the discrepancy between the theoretical and the
measured relationships between AMR and U. We used
lower swimming speeds for cod in our model since
the chub mackerel is a faster swimmer, but the general
observation that efficiency increases with swimming
speed was preserved the way we modelled . The biological interpretation of an increasing may embody
an enhanced efficiency as the number of recruited motor units increases, as well as the mechanisms by which

Tilting has strong implications for fisheries science

because target strength changes with the exposed crosssectional area of the swimbladder (MacLennan and
Simmonds, 1992). Herring, for example, undertake extensive vertical migrations during overwintering, and
these migrations are associated with large changes in
tilt angle (Huse and Ona, 1996). Our results show that
tilting could save energy, although our model predicted
energy savings of only 0.56%. This is consistent with
the relatively small optimal tilt angle of around 7 predicted by the model. Since tilting probably will be
in conflict with common behaviours such as foraging, transport, and predator avoidance, it may be seen
mostly during periods of rest or inactivity, or during
overwintering as in the case of herring.
Another feature that changes target strength of fish
is changes in swimbladder volume caused by vertical
migration (Nakken and Olsen, 1977; Ona, 1990). This
is a problem during acoustic abundance measurements
of cod at times when the cod spends a considerable
part of the day off the bottom (Rose and Porter, 1996).
In such cases, the swimbladder volume and thus target strength (the acoustic reflection measured by an
echosounder) will often be reduced deeper down since
cod is usually neutrally buoyant at the top of the vertical range. Both tilt angle and swimbladder volume can
significantly influence target strength. Our model provides predictions of swimbladder volume and tilt angle
when the vertical behaviour is known. In combination
with equations relating target strength to swimbladder
volume or shape (e.g. Ona, 1990), these predictions
can be used to improve estimates and uncertainties in
biomass estimates.
This model considers hovering and using fins as
hydrofoils (including body lift and changing the tilt
angle) as the only alternatives to swimbladder regulation. Analogous to the effects of gait transitions on
the energetic cost of terrestrial locomotion, more energetically feasible solutions may apply at different levels of under- or over-flotation. An alternative mode of
buoyancy regulation is suggested by the sawtooth like
profile sometimes seen during tracking of individual

E. Strand et al. / Ecological Modelling 185 (2005) 309327

fish on echograms. This pattern probably stems from

voluntary floating/sinking interspersed with periods of
more or less vertical swimming (Huse and Ona, 1996).
Weihs (1973) suggested that a glide (downwards) and
swim (upwards) mode of behaviour during horizontal migrations could be energetically advantageous for
continuously underflotated fish, such as fish without
swimbladders (e.g. Scombrids). This type of behaviour,
however, is to our knowledge not reported for cod, but
could be favoured in situations when fish experiences
buoyancy outside its normal range, or when e.g. fast
swimming required for hydrodynamic lift production
would make the fish conspicuous to predators.
4.5. Interpretation of eld data
The calculated swimbladder volumes and energy expenditure for the cod equipped with a data storage tag
show how the present model can aid interpretation of
observed behavioural patterns (Fig. 7ad, God and
Michalsen, 2000). The cod was likely to have foraged
at times, and thus actively swimming more or less regardless of the state of its swimbladder throughout the
period of recording. The predicted swimbladder volume dynamics and corresponding energy expenditure
do not take other possible activities into consideration.
Interestingly, the application of this model to observed
depth positions opens up for a systematic analysis of
the energetic implications of different categories of behaviour. Coupling this information with the knowledge
of cod behaviour throughout the year and in different
geographical areas can help us understand the ecological significance of these behaviours and also point
towards the evolutionary motivation that has shaped
them.

325

estimates of swimming speed can aid interpretation of

actual and optimal behaviour.
The presented model makes explicit ways in which
energetic costs and physiological constraints associated with buoyancy control influence on behaviour. The
rapidly increasing hydrostatic pressure with depth affects how readily the swimbladder can accommodate
to depth changes. As the swimbladder responds more
slowly, compensatory swimming can create lift, but
will also increase the overall cost of buoyancy regulation. The relative importance of the swimbladder and
compensatory swimming will thus shift with depth, and
the implications for behaviour will vary.
This model synthesises available information about
the swimbladder and hydrodynamic buoyancy regulation. While some aspects of fish buoyancy regulation
are well understood, it is evident that other aspects require more research. Especially, both experimental and
theoretical studies of swimbladder volume during natural behaviour and the hydrodynamics of swimming
including drag and lift are needed. The paradoxical relationship between metabolic rate and swimming speed
suggests that metabolic efficiency increases with swimming speed. The crudely modelled efficiency factor
in this paper suggests a type of solution that may
aid disentangling this complex relationship. The recent advances in thrust measures using digital particle image velocimetry (e.g. Drucker and Lauder, 1999)
are promising and may provide a more accurate description of this phenomenon. However, the difficulties
of scaling, where drag scales with absolute swimming
speed while metabolism and elastic properties scale
with body size, still push a mechanistic understanding
into the future.

Acknowledgements
5. Conclusions
According to the resolution of the time scale, it is
possible to use the equations described here to study
behaviour in varying detail. Although the numerical
estimates of energy consumption are to some degree
uncertain, it will be possible to use the qualitative estimates to compare both behavioural strategies and geographical and temporal variations from longer timeseries. In a more detailed perspective, the energetics
during daily vertical migrations in combination with

We would like to thank K. Michalsen for kindly providing us with the depth versus time data set on which
we were able to visualise the model, A.G.V. Salvanes
for data on fish fins, and I. Huse for reading and commenting the manuscript. We would also like to thank
two anonymous reviewers for valuable comments. E.S.
was supported by The Research Council of Norway
and the European Commission contract Q5RS-200200813; C.J. and G.H. were supported by The Research
Council of Norway.

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E. Strand et al. / Ecological Modelling 185 (2005) 309327

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